Abstract
Introduction
The characteristics of cervical spondylolisthesis are not currently fully understood, because of the shortage of reports covering the large population of patients with cervical spondylolisthesis. The purpose of this study was to elucidate the characteristics of cervical spondylolisthesis by examining a relatively large number of cases.
Methods
We analyzed 101 cases with more than 2 mm of vertebral listhesis as determined from X-ray or computed tomography (CT) images among 731 patients who underwent surgery at a single institute. We considered the C2-7 angle, range of motion, and C2-7 sagittal vertical axis on lateral X-ray images. From sagittal CT images, classifications into five grades based on the slipped disc and adjacent caudal levels were made. We examined the orientation of facet joints at the slipped level using axial CT images.
Results
Spondylolisthesis was recognized in 101 cases at 124 levels. Anterior and posterior spondylolisthesis were detected in 68 and 40 cases, respectively. Anterior spondylolisthesis developed predominantly at C3 or C4, usually at the level adjacent to the narrowed disc, or at C7, adjacent to the stiffened thoracic spine. The disc height was relatively preserved at the anterior slipped level. Posterior spondylolisthesis developed predominantly at the level of the significantly narrowed disc associated with advanced intervertebral osteoarthritis. At the segment with listhesis in the lower cervical spine, the direction of the facet joint in the axial plane tended to be posteromedial.
Conclusions
Cervical degenerative spondylolisthesis was classified into two types. The first and more common listhesis occurred adjacent to stiffened levels, and anterior slippage was common in this type. The second and less common listhesis occurred within progressively degenerated segments, and posterior slippage was prominent. We have uniquely described the morphological changes in orientation of the cervical facet joints at the slipped level in the transverse plane.
Keywords: cervical facet joint, spondylolisthesis, imaging, CT, X-ray
Introduction
The characteristics of cervical spondylolisthesis are not currently fully understood, because of the shortage of reports covering the large number of patients with cervical spondylolisthesis. Since the first description of cervical spondylolisthesis by Perlman and Hawes in 19511), only one study has reported the evaluation of more than 100 cases of cervical spondylolisthesis2). In 2003, Tani et al. described the functional importance of degenerative spondylolisthesis in cervical spondylotic myelopathy (CSM) by analyzing 47 spondylolisthesis patients3). In 2007, Kawasaki et al. studied 79 patients with cervical spondylolisthesis and reported that degenerative cervical spondylolisthesis of 3.5 mm or more occurred in as many as 30% of older CSM patients4). In 2009, Dean et al. analyzed 58 degenerative spondylolisthesis patients and identified two types of cervical degenerative anterior spondylolisthesis5). In 2013, Park et al. studied the natural history of 27 patients with degenerative cervical spondylolisthesis and reported that they seemed to remain stable from 2 to nearly 8 years of follow-up6). Reports concerning cervical spondylolisthesis have increased, but the research is still insufficient to clarify the pathology and proper treatment choice for this disease. The purpose of this study was to determine the characteristics of cervical spondylolisthesis by analyzing 101 patients with cervical spondylolisthesis.
Materials and Methods
Between 2008 and 2013, 731 patients underwent operations for cervical spinal disorders at a single spine center. All patients underwent conventional radiographic examinations of the cervical spine preoperatively, including lateral imaging in flexion and extension. A plain computed tomography (CT) or myelogram-CT image was taken of each patient. We defined cervical spondylolisthesis as anteroposterior vertebral slipping of more than 2 mm, identified on lateral standing X-ray images in a neutral position or on sagittal CT images according to the criteria describes in previous papers3,6-8). Motion of 1 mm or greater on flexion-extension views was considered to represent instability, according to a previous paper5). The clinical records and radiographs of spondylolisthesis patients were independently reviewed. We recruited a total of 100 asymptomatic volunteers between January 2010 and June 2010 at one radiology clinic (Utsunomiya Central Clinic). There were 20 subjects in each decade of age from the 20s to the 60s. Interestingly, there was no subject who had cervical spondylolisthesis when stood in a neutral position. We selected 20 asymptomatic volunteers in their 60s, who had plain X-ray images and magnetic resonance images of the cervical spine taken, to serve as the control group.
We evaluated intervertebral disc height according to the revised Matsumoto method9). We defined disc height grade as the percent of height reduction compared with the most adjacent normal disc on sagittal CT images, graded from 0 to 4: grade 0, no narrowing of the disc space; grade 1, less than 25% loss of height; grade 2, 25%-50% loss of height; grade 3, 50%-75% loss of height; and grade 4, more than 75% loss of height.
We classified the cervical curvature of spondylolisthesis patients and asymptomatic volunteers into five groups according to Takeshima's method10): Group A, lordosis; Group B, straight; Group C, kyphosis; Group D, sigmoid with cranial lordosis; and Group E, sigmoid with cranial kyphosis. We evaluated subchondral bone cyst formation in vertebral endplates on the segment of slippage using sagittal CT images.
Sagittal alignment of the cervical spine was measured at C2-7, using the Cobb method, on lateral radiographs of patients stood in a neutral position. Neck range of motion (ROM) was assessed based on the differences in C2-7 angles from flexion to extension. We measured the C2-7 sagittal vertical axis (SVA), which was defined as the deviation of the C2 plumb line (extending from the centroid of the C2 vertebra) from the posterior superior corner of the vertebral body of C7, with positive sagittal alignment defined as an anterior deviation.
The orientation of the superior articular surfaces from C3 (C2/3 zygapophyseal joint) to T1 was analyzed using axial CT slices according to Pal's method11). He studied dry macerated bones taken from 30 adult human male vertebral columns. He reported that, at the C2/3 facet joint level, all columns showed posteromedially facing superior articular facets, and, at the C7/T1 facet joint level and below, all columns had posterolaterally facing superior articular facets. The level at which a change in orientation from posteromedially to posterolaterally facing superior articular facets occurred was not constant. In short, he categorized facet joint orientation in relation to the transverse plane into the posteromedial, posterolateral, and transitional groups (Fig. 1).
Figure 1.
Classification of the orientation of facet joints in the axial plane.
We categorized the orientation of the facet joints in relation to the transverse plane into the posteromedial, posterolateral, and transitional groups.
Statistical analysis
We used one-way analysis of variance (ANOVA) followed by Bonferroi/Dunn's post hoc test for analyzing statistical differences in the data obtained from the X-ray images. We used the Kruskal-Wallis test followed by Bonferroi/Dunn's post hoc test for analyzing statistical differences in the disc height data. Chi-square tests were used to compare the proportions of diseases and the ratio of bone cyst formation. All statistical analyses were performed with commercially available software programs (R version 3.0.2; The R Foundation for Statistical Computing, Vienna, Austria, and StatView version 5; SAS Institute Inc., Cary, NC, USA).
Results
Epidemiology (Table 1)
Table 1.
Epidemiology of Listhesis Classified according to Disease Cause.
| A | B | C | D | E | F | |
|---|---|---|---|---|---|---|
| Number of cases | 17 | 123 | 487 | 64 | 17 | 24 |
| Number of cases with listhesis | 0 | 6 | 89 | 1 | 4 | 1 |
| Ratio of slippage (%) | 0 | 4.9 | 18.3 | 1.6 | 23.5 | 4.2 |
| Average age (yrs) | ||||||
| without listhesis | 47.9±20.6 | 61.1±9.9 | 62.8±12.6 | 49.0±10.6 | 60.8±13.0 | 58.4±19.1 |
| with listhesis | N/A | 67.7±8.1 | 70.5±9.8 | 64 | 63.0±6.1 | 71 |
A: Tumor of the spinal cord or vertebrae, B: Ossification of the longitudinal ligament, C: Cervical spondylotic amyotrophy or myelopathy, D: Cervical spondylotic radiculopathy or cervical disc herniation, E: Rheumatoid arthritis or destructive spondyloarthropathy, F: Miscellaneous diseases
We organized 731 patients into six groups according to disease type: group A, tumor of the spinal cord or vertebrae; group B, ossification of the longitudinal ligament; group C, cervical spondylotic amyotrophy or CSM; group D, cervical spondylotic radiculopathy or cervical disc herniation; group E, rheumatoid arthritis or destructive spondyloarthropathy; and group F, miscellaneous diseases.
The prevalence rate of slippage was significantly higher in groups C and F (Chi-square test, p < 0.0001). The average age of patients with spondylolisthesis was higher than that of those without spondylolisthesis in all groups.
Anterior and posterior spondylolisthesis (Table 2)
Table 2.
Comparison of Patients with and without Listhesis.
| Total without listhesis | Total with listhesis | Anterior listhesis | Posterior listhesis | |
|---|---|---|---|---|
| Number of cases | 630 | 101 | 68 | 40 |
| Average age (yrs) | 61.8±13.2 | 70.0±9.6 | 71.2±7.9 | 67.8±8.0 |
| Male: female | 464:168 | 68:33 | 42:26 | 30:10 |
| Total levels of listhesis | N/A | 124 | 81 | 43 |
The average age of patients with spondylolisthesis was significantly higher than that of those without spondylolisthesis. Instability was identified in 48 levels out of a total of 81 levels for anterior spondylolisthesis, whereas it was identified in 21 levels out of a total of 43 levels for posterior spondylolisthesis. The rate of instability was statistically the same for anterior and posterior spondylolisthesis. The numbers of cases with each slippage level are shown in Fig. 2. The numbers of duplications of listhesis are presented in Table 3. The male to female ratio is shown in Fig. 3. There was a higher female to male ratio of patients with anterior spondylolisthesis between C2 and C4 than at the other levels.
Figure 2.
Numbers of patients with anterior and posterior listhesis classified by the level of slippage.
Table 3.
Numbers of Duplications of Listhesis.
| Duplication of listhesis | Number of cases |
|---|---|
| 1 level | 78 cases |
| 2 levels | 18 cases |
| 3 levels | 5 cases |
| Anterior+posterior | 7 cases |
Figure 3.
Male to female ratio in anterior and posterior listhesis classified by the level of slippage.
Disc height grade at a segment with slippage and at the adjacent caudal segment (Fig. 4)
Figure 4.
Average disc height grade in the three groups.
In patients with anterior listhesis, the disc height at a segment with slippage was significantly higher than that at an adjacent caudal segment. Also, the disc height at an adjacent caudal segment was significantly lower than the corresponding disc height of the 20 asymptomatic subjects. This meant that anterior listhesis happened adjacent to a narrowed disc and the disc height remained higher at the segment with slippage. In patients with posterior listhesis, the disc height at a segment with slippage was significantly lower than that at an adjacent caudal segment. The disc heights at an adjacent caudal segment were not significantly different between the patients with anterior listhesis and those with posterior listhesis. This meant that disc height at a segment with posterior listhesis was significantly narrowed. Interestingly, there were no segments with slippage in the asymptomatic subjects (Fig. 4). The disc heights of patients with slippage were significantly lower than those of asymptomatic subjects (Kruskal-Wallis test, p < 0.0001).
Cervical alignment (Fig. 5)
Figure 5.
Types of alignment and the numbers of cases of each alignment in the three groups.
A: lordosis, B: straight, C: kyphosis, D: sigmoid with cranial lordosis, E: sigmoid with cranial kyphosis.
The ratio of subjects with malalignment, such as kyphosis and sigmoid curvature, was significantly higher among patients with anterior or posterior spondylolisthesis.
The ratio of subjects with malalignment, such as kyphosis and sigmoid curvature, was significantly higher among patients with anterior or posterior spondylolisthesis. Cervical malalignment significantly occurred in patients with anterior or posterior spondylolisthesis compared with asymptomatic subjects.
Subchondral bone cyst formation of vertebral endplates at a segment of slippage (Table 4)
Table 4.
Radiographic Findings for Anterior Listhesis Patients, Posterior Listhesis Patients, and Asymptomatic Volunteers.
| Anterior listhesis | Posterior listhesis | Asymptomatic volunteer | |
|---|---|---|---|
| C2-7 angle (°) | 6.2±14.7 | 11.9±15.2 | 6.9±15.9 |
| C2-7 SVA (mm) | 30.4±16.2 | 22±15.9 | 20.1±10.5 |
| C2-7 angle in flexion (°) | -13.0±13.4 | -10.4±16.2 | -16.8±9.9 |
| C2-7 angle in extension (°) | 20.7±12.6 | 24.7±15.6 | 31.7±11.5 |
| ROM (°) | 34.0±11.8 | 34.6±11.8 | 48.6±12.6 |
| Bone cyst formation | 29.6% | 86.0% | N/A |
SVA: sagittal vertical axis, ROM: range of motion
Subchondral bone cyst formation of vertebral endplates was identified more frequently on segments with posterior slippage (Chi-square test, p < 0.0001).
C2-7 angle and C2-7 SVA (Table 4)
There was no statistically significant difference in the C2-7 angle among the three groups (ANOVA, p = 0.127). The C2-7 SVA in patients with anterior listhesis was significantly higher than that of both asymptomatic volunteers and patients with posterior listhesis (ANOVA, p = 0.003).
Neck ROM and C2-7 angle in flexion and extension (Table 4)
The ROM was significantly lower in a group of patients where each patient exhibits anterior listhesis or posterior listhesis (ANOVA, p < 0.0001). The C2-7 angle in flexion was higher in patients with posterior listhesis, without a statistical difference (ANOVA, p = 0.26), while the C2-C7 angle in extension was significantly lower in patients with anterior listhesis (ANOVA, p = 0.007). This shows that neck flexion was limited in patients with posterior slippage and neck extension was limited in patients with anterior slippage.
Direction of facet joints in the transverse plane (Fig. 6)
Figure 6.
Direction of the facet joints at the slipped level in the transverse plane classified by the level and direction of listhesis compared with the distribution in Pal’s report.
We referred to Pal's results as control data for the direction of the facet joints.
Below C6, the ratio of subjects with posteromedially facing facets was significantly higher for both anterior and posterior listhesis than that in Pal's report. At the segment with anterior or posterior listhesis in the lower cervical spine, the direction of the facet joint in the axial plane tended to be posteromedial.
Discussion
Spondylolisthesis was well recognized in old patients (mean age 70) in our study, regardless of the type of underlying disease. An earlier report stated that spondylolisthesis occurred in as many as 30% of elderly CSM patients4). The findings in this study and our study suppose that spondylolisthesis was mainly induced by the degenerative cascade. Kirkaldy-Willis described the phases of lumbar spine degeneration, such as dysfunction, instability, and stabilization, which he called the degenerative cascade12). He described how the progressive degeneration of discs and facet joints leads to stretching of the adjacent capsules and ligaments; uni- or multisegmental instability then produces rotational and translational subluxation, and this finally results in degenerative spondylolisthesis or scoliosis. The mechanism of the formation of cervical spondylolisthesis may be similar to that of the lumbar form.
We clarified that anterior spondylolisthesis at C7 is a relatively common lesion. In previous papers, the most common level for cervical listhesis was reported to be C3/4 or C4/5. Spondylolisthesis below C5/6 was reportedly rare3-5,13). In our study, we demonstrated that anterior spondylolisthesis at C7/T1 and posterior spondylolisthesis at C5/6 were relatively common. Our usage of CT images might have allowed us to detect spondylolisthesis at C7/T1 in a way that was not possible for studies reported in previous papers. There was only one study which used magnetic resonance imaging (MRI) for detecting the slippage, and the researchers stated that anterior spondylolisthesis at C7 was a relatively common lesion14). CT imaging or MRI is considered to be necessary to detect the slippage at C7/T1 in many cases. The cervicothoracic junction is structurally unstable, because the mobile cervical spine connects with the relatively immobile thoracic spine15). This precariousness might accelerate degenerative changes in the disc and then induce slippage. Similar to other studies3,4), C3/4 was the most common segment for listhesis identified in our study. The pseudosubluxation in the midcervical spine reported by Penning might promote spondylolisthesis at C3/416).
Considering the results of disc height at the slipped level, we can say that anterior spondylolisthesis generally occurs at the level adjacent to the stabilized level where the disc space is narrowed, and the disc height of the slipped level is usually preserved, which allows the vertebra to slip down in flexion.
Some reports described that anterior spondylolisthesis occurred adjacent to stiff levels, because of compensatory abnormal subluxation above stiff levels5,17,18). In contrast to anterior spondylolisthesis, posterior spondylolisthesis occurred predominantly at the level where the disc height significantly narrowed and bone cyst formation was well recognized. This implies that posterior spondylolisthesis is a result of advanced disc degeneration. An earlier report described the typical radiological appearance of degenerative retrolisthesis, including the narrowing of an intervertebral disc, which is occasionally associated with degenerative changes of the involved facets7).
We can say that cervical degenerative spondylolisthesis could be classified into two types. The first and more common listhesis occurred adjacent to stiffened levels, and anterior slippage was common in this type. The second and less common listhesis occurred within progressively degenerated segments, and posterior slippage was prominent. There is so far only one previous report which has mentioned two types of anterior cervical spondylolisthesis5).
We have uniquely described the morphological changes in the orientation of cervical facet joints at the slipped level in the transverse plane for cervical spondylolisthesis. In contrast to papers concerning the cervical spine, there are many papers which have described predisposing factors for degenerative lumbar spondylolisthesis, such as the sagittal orientation of lumbar facet joints, hormonal factors, ligament hyperlaxity, and iliolumbar morphology19). When there is a morphological difference between the cervical facet joints at each level, the motion pattern of each level differs according to the facet joint shape11). The unusual shape of the facet joints inhibits natural movement or causes abnormal movement, which finally may induce spondylolisthesis. However, the observed morphological differences in the cervical facet joints were possibly only the consequence of deformities induced by slippage. To discover whether the morphological differences in the facet joints are the cause or the outcome, a longitudinal study is necessary.
Limitations
As with any study, this investigation has several limitations. First, it is a retrospective study including a small number of patients and asymptomatic volunteers. Our research would be improved by performing a prospective study that utilizes a large number of subjects. Second, we did not describe in detail the clinical presentation and treatment options. To understand the precise pathology of spondylolisthesis, we have to clarify information such as what symptoms patients presented with and what types of surgery are effective for treating spondylolisthesis. We will elucidate the importance of cervical listhesis on surgical outcomes in the future. Third, the diversity of diseases included in this study might have influenced the outcome of our study. Fourth, we selected patients who underwent surgery only. To elucidate the overall characteristics of spondylolisthesis, we should include some of the many cases of mild spondylosis or even asymptomatic subjects. Fifth, our study insufficiently considered dynamic factors. Dynamic translation of the spine is indispensable in understanding the pathology of cervical spine diseases. Nevertheless, we defined spondylolisthesis by using neutral lateral X-ray images, because it was an adequate way to identify symptomatic spondylolisthesis. Of the 100 asymptomatic volunteers, no one had cervical spondylolisthesis while standing in a neutral position; therefore, we reasoned that examining spondylolisthesis with patients stood in a neutral position was appropriate for our investigation. The cervical spine is an inherently mobile organ16); therefore, the determination of cervical instability is a difficult problem. Cervical spondylolisthesis in a flexed or extended neck position possibly suggests inherent instability of the cervical spine. In order to elucidate the importance of dynamic listhesis, we need to conduct further study, utilizing a large number of subjects. Addressing these aspects would improve our research.
Conclusion
Anterior spondylolisthesis tended to occur at the level adjacent to the stabilized level, where the disc space was narrowed due to degeneration, or at the cervicothoracic junction, where the thoracic spine is naturally stiffened. The disc height of the slipped level was usually preserved, thus presenting an opportunity for the vertebra to slip down in flexion. Posterior spondylolisthesis tended to occur at the level where the disc space was significantly narrowed and cyst formation was often detected. This suggests that posterior spondylolisthesis is related to intervertebral disc degeneration. Furthermore, the direction or orientation of the facet joints may influence spondylolisthesis.
Conflicts of Interest: The authors declare that there are no conflicts of interest.
References
- 1.Perlman R, Hawes LE. Cervical spondylolisthesis. J Bone Joint Surg Am. 1951; 33-A(4): 1012-3. [PubMed] [Google Scholar]
- 2.Pellengahr C, Pfahler M, Kuhr M, et al. Influence of facet joint angles and asymmetric disk collapse on degenerative olisthesis of the cervical spine. Orthopedics. 2000;23(7):697-701. [DOI] [PubMed] [Google Scholar]
- 3.Tani T, Kawasaki M, Taniguchi S, et al. Functional importance of degenerative spondylolisthesis in cervical spondylotic myelopathy in the elderly. Spine (Phila Pa 1976). 2003;28(11):1128-34. [DOI] [PubMed] [Google Scholar]
- 4.Kawasaki M, Tani T, Ushida T, et al. Anterolisthesis and retrolisthesis of the cervical spine in cervical spondylotic myelopathy in the elderly. J Orthop Sci. 2007;12(3):207-13. [DOI] [PubMed] [Google Scholar]
- 5.Dean CL, Gabriel JP, Cassinelli EH, et al. Degenerative spondylolisthesis of the cervical spine: analysis of 58 patients treated with anterior cervical decompression and fusion. Spine J. 2009;9(6):439-46. [DOI] [PubMed] [Google Scholar]
- 6.Park MS, Moon SH, Lee HM, et al. The natural history of degenerative spondylolisthesis of the cervical spine with 2- to 7-year follow-up. Spine (Phila Pa 1976). 2013;38(4):E205-10. [DOI] [PubMed] [Google Scholar]
- 7.Lee C, Woodring JH, Rogers LF, et al. The radiographic distinction of degenerative slippage (spondylolisthesis and retrolisthesis) from traumatic slippage of the cervical spine. Skeletal Radiol. 1986;15(6):439-43. [DOI] [PubMed] [Google Scholar]
- 8.Jun HS, Kim JH, Ahn JH, et al. T1 slope and degenerative cervical spondylolisthesis. Spine (Phila Pa 1976). 2015;40(4):E220-6. [DOI] [PubMed] [Google Scholar]
- 9.Matsumoto M, Fujimura Y, Suzuki N, et al. MRI of cervical intervertebral discs in asymptomatic subjects. J Bone Joint Surg Br. 1998;80(1):19-24. [DOI] [PubMed] [Google Scholar]
- 10.Takeshima T, Omokawa S, Takaoka T, et al. Sagittal alignment of cervical flexion and extension: lateral radiographic analysis. Spine (Phila Pa 1976). 2002;27(15):E348-55. [DOI] [PubMed] [Google Scholar]
- 11.Pal GP, Routal RV, Saggu SK. The orientation of the articular facets of the zygapophyseal joints at the cervical and upper thoracic region. J Anat. 2001;198(Pt 4):431-41. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Kirkaldy-Willis WH, Farfan HF. Instability of the lumbar spine. Clin Orthop Relat Res. 1982(165):110-23. [PubMed] [Google Scholar]
- 13.Jiang SD, Jiang LS, Dai LY. Degenerative cervical spondylolisthesis: a systematic review. Int Orthop. 2011;35(6):869-75. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Suzuki A, Daubs MD, Inoue H, et al. Prevalence and motion characteristics of degenerative cervical spondylolisthesis in the symptomatic adult. Spine (Phila Pa 1976). 2013;38(17):E1115-20. [DOI] [PubMed] [Google Scholar]
- 15.An HS, Vaccaro A, Cotler JM, et al. Spinal disorders at the cervicothoracic junction. Spine (Phila Pa 1976). 1994;19(22):2557-64. [DOI] [PubMed] [Google Scholar]
- 16.Penning L. Normal movements of the cervical spine. AJR Am J Roentgenol. 1978;130(2):317-26. [DOI] [PubMed] [Google Scholar]
- 17.Bohlman HH. Cervical Spondylosis with Moderate to Severe Myelopathy: A Report of Seventeen Cases Treated by Robinson Anterior Cervical Discectomy and Fusion. Spine. 1977;2(2):151-62. [Google Scholar]
- 18.Deburge A, Mazda K, Guigui P. Unstable degenerative spondylolisthesis of the cervical spine. J Bone Joint Surg Br. 1995;77(1):122-5. [PubMed] [Google Scholar]
- 19.Matsunaga S, Sakou T, Morizono Y, et al. Natural history of degenerative spondylolisthesis. Pathogenesis and natural course of the slippage. Spine (Phila Pa 1976). 1990;15(11):1204-10. [DOI] [PubMed] [Google Scholar]